Brown Algal Model Organisms.

Model organisms are extensively used in research as accessible and convenient systems for studying a particular area or question in biology. Traditionally, only a limited number of organisms have been studied in detail, but modern genomic tools are enabling researchers to extend beyond the set of classical model organisms to include novel species from less-studied phylogenetic groups. This review focuses on model species for an important group of multicellular organisms, the brown algae. The development of genetic and genomic tools for the filamentous brown alga Ectocarpus has led to it emerging as a general model system for this group, but additional models, such as Fucus or Dictyota dichotoma, remain of interest for specific biological questions. In addition, Saccharina japonica has emerged as a model system to directly address applied questions related to algal aquaculture. We discuss the past, present, and future of brown algal model organisms in relation to the opportunities and challenges in brown algal research.

Insights into the molecular bases of multicellular development from brown algae.

The transition from simple to complex multicellularity represents a major evolutionary step that occurred in only a few eukaryotic lineages. Comparative analyses of these lineages provide insights into the molecular and cellular mechanisms driving this transition, but limited understanding of the biology of some complex multicellular lineages, such as brown algae, has hampered progress. This Review explores how recent advances in genetic and genomic technologies now allow detailed investigations into the molecular bases of brown algae development. We highlight how forward genetic techniques have identified mutants that enhance our understanding of pattern formation and sexual differentiation in these organisms. Additionally, the existence and nature of morphogens in brown algae and the potential influence of the microbiome in key developmental processes are examined. Outstanding questions, such as the identity of master regulators, the definition and characterization of cell types, and the molecular bases of developmental plasticity are discussed, with insights into how recent technical advances could provide answers. Overall, this Review highlights how brown algae are emerging as alternative model organisms, contributing to our understanding of the evolution of multicellular life and the diversity of body plans.

The baseless mutant links protein phosphatase 2A with basal cell identity in the brown alga Ectocarpus.

The first mitotic division of the initial cell is a key event in all multicellular organisms and is associated with the establishment of major developmental axes and cell fates. The brown alga Ectocarpus has a haploid-diploid life cycle that involves the development of two multicellular generations: the sporophyte and the gametophyte. Each generation deploys a distinct developmental programme autonomously from an initial cell, the first cell division of which sets up the future body pattern. Here, we show that mutations in the BASELESS (BAS) gene result in multiple cellular defects during the first cell division and subsequent failure to produce basal structures during both generations. BAS encodes a type B″ regulatory subunit of protein phosphatase 2A (PP2A), and transcriptomic analysis identified potential effector genes that may be involved in determining basal cell fate. The bas mutant phenotype is very similar to that observed in distag (dis) mutants, which lack a functional Tubulin-binding co-factor Cd1 (TBCCd1) protein, indicating that TBCCd1 and PP2A are two essential components of the cellular machinery that regulates the first cell division and mediates basal cell fate determination.

Assembly and synthesis of the extracellular matrix in brown algae.

In brown algae, the extracellular matrix (ECM) and its constitutive polymers play crucial roles in specialized functions, including algal growth and development. In this review we offer an integrative view of ECM construction in brown algae. We briefly report the chemical composition of its main constituents, and how these are interlinked in a structural model. We examine the ECM assembly at the tissue and cell level, with consideration on its structure in vivo and on the putative subcellular sites for the synthesis of its main constituents. We further discuss the biosynthetic pathways of two major polysaccharides, alginates and sulfated fucans, and the progress made beyond the candidate genes with the biochemical validation of encoded proteins. Key enzymes involved in the elongation of the glycan chains are still unknown and predictions have been made at the gene level. Here, we offer a re-examination of some glycosyltransferases and sulfotransferases from published genomes. Overall, our analysis suggests novel investigations to be performed at both the cellular and biochemical levels. First, to depict the location of polysaccharide structures in tissues. Secondly, to identify putative actors in the ECM synthesis to be functionally studied in the future.

Brown algal cell walls and development.

Brown algae are complex multicellular eukaryotes whose cells possess a cell wall, which is an important structure that regulates cell size and shape. Alginate and fucose-containing sulfated polysaccharides (FCSPs) are two carbohydrate types that have major roles in influencing the mechanical properties of the cell wall (i.e. increasing or decreasing wall stiffness), which in turn regulate cell expansion, division, adhesion, and other processes; however, how brown algal cell wall structure regulates its mechanical properties, and how this relationship influences cellular growth and organismal development, is not well-understood. This chapter is focused on reviewing what we currently know about how the roles of alginates and FCSPs in brown algal developmental processes, as well as how they influence the structural and mechanical properties of cell walls. Additionally, we discuss how brown algal mutants may be leveraged to learn more about the underlying mechanisms that regulate cell wall structure, mechanics, and developmental processes, and finally we propose questions to guide future research with the use of emerging technologies.

From viruses to humans - Exploring the structure-function relationship of the Kesv protein for the future of biomedicine.

Viruses often use ion channel proteins to initialise host infections. Defects in ion channel proteins are also linked to several metabolic disorders in humans. In that instance, modulation of ion channel activities becomes central to development of antiviral therapies and drug design. Kesv, a potassium-selective ion channel protein expressed by Ectocarpus siliculosus virus (EsV), possesses remarkable properties which can help to characterise the molecular basis of the functional processes relevant to virus biology and human physiology. The small structural features of this ion channel could serve as a fundamental primer to study more complex ion channels from humans. Therefore, in spite of their evolutionary distance, the potential link between viral and human ion channel proteins could provide opportunities for therapeutic and biotechnological applications.

Aldehyde perception induces specific molecular responses in Laminaria digitata and affects algal consumption by a specialist grazer.

In the marine environment, distance signaling based on water-borne cues occurs during interactions between macroalgae and herbivores. In the brown alga Laminaria digitata from North-Atlantic Brittany, oligoalginates elicitation or grazing was shown to induce chemical and transcriptomic regulations, as well as emission of a wide range of volatile aldehydes, but their biological roles as potential defense or warning signals in response to herbivores remain unknown. In this context, bioassays using the limpet Patella pellucida and L. digitata were carried out for determining the effects of algal transient incubation with 4-hydroxyhexenal (4-HHE), 4-hydroxynonenal (4-HNE) and dodecadienal on algal consumption by grazers. Simultaneously, we have developed metabolomic and transcriptomic approaches to study algal molecular responses after treatments of L. digitata with these chemical compounds. The results indicated that, unlike the treatment of the plantlets with 4-HNE or dodecadienal, treatment with 4-HHE decreases algal consumption by herbivores at 100 ng.ml-1 . Moreover, we showed that algal metabolome was significantly modified according to the type of aldehydes, and more specifically the metabolite pathways linked to fatty acid degradation. RNAseq analysis further showed that 4-HHE at 100 ng.ml-1 can activate the regulation of genes related to oxylipin signaling pathways and specific responses, compared to oligoalginates elicitation. As kelp beds constitute complex ecosystems consisting of habitat and food source for marine herbivores, the algal perception of specific aldehydes leading to targeted molecular regulations could have an important biological role on kelps/grazers interactions.

Exon shuffling potentiates a diverse repertoire of brown algal NB-ARC-TPR candidate immune receptor proteins via alternative splicing.

Like other organisms, brown algae are subject to diseases caused by bacteria, fungi, and viruses. Brown algal immunity mechanisms are not well characterized; however, there is evidence suggesting that pathogen receptors exist in brown algae. One key protein family likely associated with brown algal innate immunity possesses an NB-ARC domain analogous to innate immune proteins in plants and animals. In this study, we conducted an extensive survey of NB-ARC genes in brown algae and obtained insights into the domain organization and evolutionary history of the encoded proteins. Our data show that brown algae possess an ancient NB-ARC-tetratricopeptide repeat (NB-TPR) domain architecture. We identified an N-terminal effector domain, the four-helix bundle, which was not previously found associated with NB-ARC domains. The phylogenetic tree including NB-ARC domains from all kingdoms of life suggests the three clades of brown algal NB-TPRs are likely monophyletic, whereas their TPRs seem to have distinct origins. One group of TPRs exhibit intense exon shuffling, with various alternative splicing and diversifying selection acting on them, suggesting exon shuffling is an important mechanism for evolving ligand-binding specificities. The reconciliation of gene duplication and loss events of the NB-ARC genes reveals that more independent gene gains than losses have occurred during brown algal evolution, and that tandem duplication has played a major role in the expansion of NB-ARC genes. Our results substantially enhance our understanding of the evolutionary history and exon shuffling mechanisms of the candidate innate immune repertoire of brown algae.

Low Spontaneous Mutation Rate in Complex Multicellular Eukaryotes with a Haploid-Diploid Life Cycle.

The spontaneous mutation rate µ is a crucial parameter to understand evolution and biodiversity. Mutation rates are highly variable across species, suggesting that µ is susceptible to selection and drift and that species life cycle and life history may impact its evolution. In particular, asexual reproduction and haploid selection are expected to affect the mutation rate, but very little empirical data are available to test this expectation. Here, we sequence 30 genomes of a parent-offspring pedigree in the model brown alga Ectocarpus sp.7, and 137 genomes of an interspecific cross of the closely related brown alga Scytosiphon to have access to the spontaneous mutation rate of representative organisms of a complex multicellular eukaryotic lineage outside animals and plants, and to evaluate the potential impact of life cycle on the mutation rate. Brown algae alternate between a haploid and a diploid stage, both multicellular and free living, and utilize both sexual and asexual reproduction. They are, therefore, excellent models to empirically test expectations of the effect of asexual reproduction and haploid selection on mutation rate evolution. We estimate that Ectocarpus has a base substitution rate of µbs = 4.07 × 10-10 per site per generation, whereas the Scytosiphon interspecific cross had µbs = 1.22 × 10-9. Overall, our estimations suggest that these brown algae, despite being multicellular complex eukaryotes, have unusually low mutation rates. In Ectocarpus, effective population size (Ne) could not entirely explain the low µbs. We propose that the haploid-diploid life cycle, combined with extensive asexual reproduction, may be additional key drivers of the mutation rate in these organisms.

Algal Sex Determination and the Evolution of Anisogamy.

Algae are photosynthetic eukaryotes whose taxonomic breadth covers a range of life histories, degrees of cellular and developmental complexity, and diverse patterns of sexual reproduction. These patterns include haploid- and diploid-phase sex determination, isogamous mating systems, and dimorphic sexes. Despite the ubiquity of sexual reproduction in algae, their mating-type-determination and sex-determination mechanisms have been investigated in only a limited number of representatives. These include volvocine green algae, where sexual cycles and sex-determining mechanisms have shed light on the transition from mating types to sexes, and brown algae, which are a model for UV sex chromosome evolution in the context of a complex haplodiplontic life cycle. Recent advances in genomics have aided progress in understanding sexual cycles in less-studied taxa including ulvophyte, charophyte, and prasinophyte green algae, as well as in diatoms.